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Ann Thorac Surg 2005;79:1691-1696
© 2005 The Society of Thoracic Surgeons

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Original articles: General thoracic

Resection of Locally Advanced (T4) Non-Small Cell Lung Cancer With Cardiopulmonary Bypass

Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation, Hôpital Marie-Lannelongue, Le Plessis-Robinson, France

Accepted for publication October 14, 2004.

^_* Address reprint requests to Dr Dartevelle, Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation, Hôpital Marie-Lannelongue, 133 Avenue de la Résistance, 92350 Le Plessis-Robinson, France (E-mail: pdartevelle{at}ccml.com).

	Abstract

Top Abstract Introduction Material and Methods Results Comment References

 
BACKGROUND: Resection of T4 non-small cell lung cancer (NSCLC) on cardiopulmonary bypass (CPB) has rarely been reported in the literature. Hence, we have reviewed our experience in the role of CPB for the surgical treatment of locally advanced NSCLC.

METHODS: All patients undergoing lung resection for bronchogenic carcinoma on CPB in our institution between January 1998 and June 2004 were reviewed.

RESULTS: Seven patients underwent lung resections on CPB for bronchogenic carcinoma during the study period. Cardiopulmonary bypass was performed for tumors invading the subclavian artery down to the aortic arch (n = 2), the descending aorta (n = 1), or the origin of the left pulmonary artery with the left atrium (n = 2). All patients were discharged home after 9 to 21 days (median, 15 days). In the long term, 2 patients are alive without recurrence 17 and 25 months after their operations, and 3 are alive with recurrence 8, 13, and 54 months postoperatively. Two additional patients required CPB while undergoing carinal resection for difficulty ventilating the left lung. Both patients had a difficult postoperative course, but were eventually discharged from hospital. One patient died without recurrence 6 months later, and the other is alive without recurrence after 72 months.

CONCLUSIONS: This study confirms the safety of CPB for NSCLC invading the great vessels and/or the left atrium in well-selected patients, and its utility when pulmonary edema develops during carinal resection. Further studies, however, are required to confirm long-term survival.

	Introduction

Top Abstract Introduction Material and Methods Results Comment References

 
Bronchogenic carcinoma continues to be a major health issue. Although surgery remains the treatment of choice, combination of surgery with chemotherapy and radiotherapy may be associated with improved survival for advanced stage non-small cell lung carcinoma (NSCLC) [1]. Locally advanced tumors (T4) invading the carina, superior vena cava, or the thoracic inlet can achieve survival rates of 30% to 40% if no mediastinal lymph node metastases are present and complete resection is achieved [2, 3]. Resection of T4 NSCLC with the use of cardiopulmonary bypass (CPB) has rarely been reported in the literature. Hence, we have reviewed the role of CPB in the surgical treatment of locally advanced bronchogenic carcinoma at Hospital Marie-Lannelongue over the past 6.5 years.

	Material and Methods

Top Abstract Introduction Material and Methods Results Comment References

 
All patients undergoing lung resection for bronchogenic carcinoma with CPB at Hospital Marie-Lannelongue between January 1998 and June 2004 were retrospectively identified and reviewed. Patients undergoing lung resection on CPB for histology other than bronchogenic carcinoma were excluded. Patients with T4 NSCLC invading the adventitia of the aorta or the left atrium, but resected without the use of CPB were also excluded from the study.

Data on demographics, signs, and symptoms at presentation, preoperative evaluation, and induction and/or adjuvant therapy were collected. Tumor characteristics, histologic features, and operative details were recorded. All complications were noted. Follow-up was complete for all patients. Site of recurrence was noted along with overall survival.

	Results

Top Abstract Introduction Material and Methods Results Comment References

 
Seven patients underwent lung resections on CPB for locally advanced bronchogenic carcinoma. Cardiopulmonary bypass was performed for tumors invading the subclavian artery down to the aortic arch (n = 2), the descending aorta (n = 1), the main pulmonary artery with the left atrium (n = 2), or the carina (n = 2). Patient demographics are presented in Table 1 and operative results in Table 2.

Resection of Left Subclavian Artery and Distal Aortic Arch
Patients 1 and 2 presented with a large tumor of the superior sulcus invading the thoracic inlet and the subclavian artery down to the distal aortic arch (Fig 1). The preoperative workup was completed by an angiography of the aortic arch and supraaortic trunks as well as a transesophageal ultrasound that demonstrated the invasion of the left subclavian artery but no involvement of the esophageal wall. Duplex scan of both carotid and vertebral arteries was also performed to assure good patency of all four vessels. Magnetic resonance imaging (MRI) was performed for the second patient to exclude an invasion of the intervertebral foramen at the level of T2 and T3.

View larger version (88K): [in this window] [in a new window]   Fig 1. Computed tomographic scan (A) and magnetic resonance imaging (B) of patient 2 showing a large tumor of the superior sulcus invading the left subclavian artery down to the aortic arch.

View larger version (70K): [in this window] [in a new window]   Fig 2. Angiography of patient 2 before (A) and after (B) surgery showing that the left subclavian artery was sectioned and anastomosed in a terminolateral fashion to the left carotid artery and the distal aortic arch was replaced with a Dacron graft.

The second patient had no involvement of the thoracic inlet beside the left subclavian artery. Hence, the left subclavian artery was sectioned distally to the tumor and anastomosed to the left carotid artery without removing the clavicle. The operation was then completed through a left posterolateral thoracotomy. A left upper lobectomy, along with resection of the aortic arch, left subclavian artery, and prevertebral muscles from T2 to T3, was performed. Cardiopulmonary bypass was initiated between the main pulmonary artery and the descending aorta. The aorta was cross-clamped between the origin of the left carotid artery and the descending aorta, and the aortic arch was reconstructed with a Dacron graft (Fig 2). Cross-clamped time lasted 20 minutes and CPB 23 minutes. Resection was complete (R0) in both patients.

Resection of Descending Aorta
Patient 3 planned to have a left pneumonectomy through a posterolateral thoracotomy. However, the tumor was found to be invading the media of the descending aorta. The patient, being positioned in a right lateral decubitus, was placed under CPB with the venous cannula in the main pulmonary artery and the arterial cannula in the descending aorta, distally to the tumor. The descending aorta was cross-clamped proximally and distally to the tumor and resected on approximately 4 cm. A Dacron graft was used for reconstruction. The CPB lasted 29 minutes. Despite complete microscopic resection of the aorta, microscopic foci of carcinoma were unexpectedly observed in the cross-section of the pulmonary artery on final histologic examination (R1 resection).

Resection of Pulmonary Artery Bifurcation and Left Atrium
Patients 4 and 5 were found to have a large tumor occluding the left main pulmonary artery at its origin, and precluding any resection of the pulmonary artery without having to reconstruct the main pulmonary artery (Fig 3). The tumor also extended into the left atrium and into the left main bronchus (1.7 cm from the carina) in patient 5.

View larger version (78K): [in this window] [in a new window]   Fig 3. Computed tomographic scan (A) and angiography (B) of patient 4 showing a large tumor occluding the left pulmonary artery at its origin. A left pneumonectomy was performed on cardiopulmonary bypass through a median sternotomy in order to be able to section the left pulmonary artery at its bifurcation.

Patient 5 required dissection of the right pulmonary artery to approach the carina and to allow stapling of the left main bronchus at its origin. The left atrium was then stapled at distance from the ostium of the pulmonary veins in order to obtain complete resection of the tumor extending into the left atrium. The CPB lasted 70 minutes; resection was complete (R0).

Resection of Carina
Patients 6 and 7 underwent carinal resection through a right posterolateral thoracotomy. Patient 6 was undergoing completion of right pneumonectomy with carinal resection for a recurrent squamous cell carcinoma, and patient 7 was undergoing carinal resection with reimplantation of the right and left main stem bronchi into the trachea for a squamous cell carcinoma of the carina. In both cases, ventilation of the left lung through the operating field became difficult because of pulmonary edema. Hence, CPB was initiated between the right atrium and the ascending aorta to allow completion of the tracheal anastomosis. The CPB lasted 70 minutes in patient 6, and 61 minutes in patient 7; resection was complete (R0) in both patients.

Postoperative Course
Both patients undergoing carinal resection under CPB had a difficult postoperative course. Pulmonary edema evolved towards acute respiratory distress syndrome (ARDS) in patient 6 and pneumonia in patient 7. Patient 7 eventually was extubated after 7 days and was discharged home on postoperative day 25. Patient 6 remained in hospital for 91 days and was eventually discharged home.

The remaining 5 patients undergoing resection of the aorta or proximal pulmonary artery with or without the left atrium were extubated after a median of 1 day (range, 0 to 3 days) and stayed in hospital for 15 days postoperatively (range, 9 to 21 days). The main complication was atelectasis of the left lower lobe associated with left recurrent nerve palsy in patient 1 (Table 2).

Outcome
Among the 5 patients undergoing resection of the aorta or proximal pulmonary artery with or without the left atrium, 2 are alive without recurrence 17 and 25 months after their operation. The remaining 3 patients are alive with recurrence 8, 13, and 54 months postoperatively. One of the two patients who underwent carinal resection on CPB died of pulmonary emboli 6 months after surgery without any signs of recurrence at autopsy (patient 6). The other is alive without recurrence 72 months after the operation.

Two patients presenting with recurrence developed brain metastasis initially. The first patient (patient 2) developed brain metastasis after 12 months and was treated with stereotactic radiosurgery. The second patient (patient 5) developed brain metastases 42 months after surgery and lung metastases 8 months later, and is currently undergoing palliative chemotherapy. The third patient (patient 3) developed skin metastases at 8 months follow-up and is currently undergoing chemotherapy.

	Comment

Top Abstract Introduction Material and Methods Results Comment References

 
The value of CPB has been reported for thoracic malignancies invading the heart or great vessels [4, 5]. However, few authors have reported their experience with CPB in lung cancer. In most patients, locally advanced bronchogenic carcinoma can be resected without the need of CPB. Tsuchiya and colleagues [6] reported a series of 101 patients with lung cancer invading the left atrium or great vessels and only 7 of them required CPB to achieve complete resection. In our experience, we have used CPB in 7 patients. Cardiopulmonary bypass was used to resect carcinoma invading the aortic arch, the descending aorta, the pulmonary artery bifurcation, the left atrium, and the carina.

Aortic invasion by NSCLC is usually limited to the adventitia. However, in rare instances, the media of the aorta is also invaded and resection requires cross-clamping of the aorta proximally and distally to remove the infiltrated wall. Some authors [6, 7] have suggested using a shunt prosthesis between the ascending and descending aorta in order to resect and reconstruct the infiltrated portion of the aorta. In our experience, and in that of others, we have found that CPB was the easiest way to achieve perfusion of the upper and lower part of the body during aortic cross-clamping [8]. We inserted the cannulas for CPB in the main pulmonary artery and the descending aorta. Perfusion of the upper part of the body was thus achieved by the beating heart and the lower part of the body was perfused by normothermic partial bypass. Adequate perfusion of the upper part of the body was controlled with an arterial line in the right radial artery. The aorta could then be cross-clamped between the innominate artery and the left carotid artery to resect the distal part of the aortic arch and the origin of the subclavian artery. Cannulation of the main pulmonary artery and descending aorta through a left posterolateral thoracotomy can also be useful when the aortic wall of the descending aorta is unexpectedly invaded by the tumor and the femoral vessels are not kept in the operating field. Using this technique, the venous cannula should be placed proximally in the left pulmonary artery after having cut the arterial ligament, and the tip of the venous cannula should be placed in the main pulmonary artery or in the right ventricle. Care should be taken to avoid placing the tip of the cannula in the right pulmonary artery, since it may prevent adequate ejection from the right ventricle. When the tumor invades the aortic arch more proximally than the left carotid artery, or if the lesser curvature of the aortic arch is invaded, CPB with selective cerebral perfusion or with circulatory arrest can be required [9, 10].

Cardiopulmonary bypass can also be useful to resect the left atrium or the origin of the left pulmonary artery. In most cases, however, resection of the left atrium can be achieved by apposing a vascular clamp on the left atrium to remove the tumor along with both pulmonary veins and by directly suturing the defect. If a larger portion of the left atrium is invaded, the tumor is often not completely resectable because of prolonged microscopic infiltration of the myocardium. Thus, CPB has rarely been used for left atrial resection in our experience. Some authors have found that CPB could be useful if the tumor extends into the lumen of the left atrium with a risk of systemic tumor embolization. Cardiopulmonary bypass allowed opening the left atrium after aortic cross-clamping and instillation of cardioplegia or after the induction of hypothermic ventricular fibrillation to avoid air embolism [11, 12].

Resection of the trachea or carinal trachea with airway reconstruction must be performed without CPB regardless of the side of the primary tumor. In our experience, we have performed approximately 100 carinal resections for bronchogenic carcinoma located on the right or on the left side and only 2 patients required CPB. In both patients, CPB was required because of difficulty ventilating the left lung due to the development of an intraoperative pulmonary edema. Cardiopulmonary bypass allowed completion of the tracheal anastomoses without tension on the suture lines from the left lung during the anastomosis. The postoperative course was difficult, but eventually both patients were discharged from the hospital, and one is alive 6 years later. Hence, if pulmonary edema of the contralateral lung develops during carinal pneumonectomy, CPB should be started early during the procedure in order to avoid further lung injury from mechanical ventilation and to be able to perform the tracheal anastomosis without tension on the suture lines.

Lung resection on CPB for locally advanced NSCLC should be performed only in well-selected patients with no mediastinal lymph node metastasis because of the risk of postoperative complications and the limited number of patients alive in the long-term after such procedures. In our experience, all patients were less than 60 years old in good clinical conditions with no medical comorbidities. With the exception of the 2 patients who unexpectedly were put on CPB for carinal resection, the remaining 5 patients did well postoperatively. They were ventilated for less than 3 days and were discharged from the hospital after a mean of 15 days.

The use of CPB does not appear to increase the risk of cancer dissemination. Klepetko and colleagues [8] reported 2 out of 5 patients alive with no evidence of disease 50 and 14 months after reconstruction of the aorta under CPB, and Horita and colleagues [13] reported one patient alive greater than 5 years after resection of the aortic arch under hypothermic circulatory arrest, despite the absence of adjuvant or neoadjuvant therapy. Several series have also reported combining lung resection for bronchogenic carcinoma with aortocoronary bypass surgery during the same operative procedure with good early and long-term results despite the use of CPB [14, 15].

Long-term outcome of patients with locally advanced lung cancer depends primarily of completeness of resection. Martini and colleagues [16] have reported a series of lung cancer invading the mediastinum, and observed that the 5-year survival rate was 30% if the tumor was completely resected, whereas it was only 14% if it was incompletely resected. Other authors [6, 17] made similar observations in a series of lung cancer invading the heart or great vessels with 5-year survival ranging between 23% and 40% if the tumor was completely resected, whereas no patients survived greater than 3 years if the tumor was incompletely resected. Further studies will be necessary to confirm these findings in patients undergoing resection of locally advanced NSCLC under CPB.

In conclusion, this study confirms the safety of CPB for NSCLC invading the great vessels and/or the left atrium in well-selected cases, and its utility when pulmonary edema develops during carinal resection. However, further follow-up and more cases are required to confirm long-term survival.

	References

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